From commensalism to parasitism in Carapidae (Ophidiiformes): heterochronic modes of development?

Abstract

Phenotypic variations allow a lineage to move into new regions of the adaptive landscape. The purpose of this study is to analyse the life history of the pearlfishes (Carapinae) in a phylogenetic framework and particularly to highlight the evolution of parasite and commensal ways of life. Furthermore, we investigate the skull anatomy of parasites and commensals and discuss the developmental process that would explain the passage from one form to the other. The genus Carapus forms a paraphyletic grouping in contrast to the genus Encheliophis, which forms a monophyletic cluster. The combination of phylogenetic, morphologic and ontogenetic data clearly indicates that parasitic species derive from commensal species and do not constitute an iterative evolution from free-living forms. Although the head morphology of Carapus species differs completely from Encheliophis, C. homei is the sister group of the parasites. Interestingly, morphological characteristics allowing the establishment of the relation between Carapus homei and Encheliophis spp. concern the sound-producing mechanism, which can explain the diversification of the taxon but not the acquisition of the parasite morphotype. Carapus homei already has the sound-producing mechanism typically found in the parasite form but still has a commensal way of life and the corresponding head structure. Moreover, comparisons between the larval and adult Carapini highlight that the adult morphotype “Encheliophis” is obtained by going beyond the adult stage reached by Carapus. The entrance into the new adaptive landscape could have been realised by at least two processes: paedomorphosis and allometric repatterning.

Taxonomic validation of Encheliophis chardewalli with description of calling abilities

“…The cylindrical swimbladder, extending from the 3rd vertebra to the 14th vertebra, is divided into three regions. The primary sound producing muscle is particularly long in this species: its origin is on the anterior upper wall of the orbit, at the level of the lateral ethmoid, and it inserts with a tendon directly on the anterior swimbladder without a hook (Parmentier et al, ; Parmentier, Lanterbecq et al, ). As usual in this taxa, the swimbladder fenestra, the second region, is situated just under the swim bladder plate and is thinner than surrounding regions.…”

“…Later, the tenuis larva increases in length substantially before a deep metamorphosis (within the host) that includes a shortening of the body (Parmentier, Lecchini, & Vandewalle, ; Parmentier, ), leading to the juvenile stage (Padoa, ; Arnold, ; Parmentier, Lecchini, Lagardere, & Vandewalle, ) before the sexually mature adults. The anatomy and the small body size associated with the straight body diameter suggest the adults still have the morphology of the tenuis (Parmentier, Lanterbecq et al, ).…”

Sound production and sonic apparatus in deep-living cusk-eels (Genypterus chilensis and Genypterus maculatus)

“…These features clearly support the importance of sonic communication in the Ophidiiformes (Fine et al, 2018(Fine et al, , 2007Nguyen et al, 2008). Since many species live in deep water (Nielsen et al, 1999) sound recordings have only been made for a few shallow species from the Carapidae (Kéver et al, 2014c;Parmentier et al, 2016aParmentier et al, , 2016bParmentier et al, , 2018bParmentier et al, , 2003 and Ophidiidae (Kéver et al, 2016Mooney et al, 2016;Rountree and Bowers-Altman, 2002).…”

“…Among potential callers in deep environments, Ophidiiform species are good candidates for several reasons. Sound-producing mechanisms 1) are found in all but one species examined to date (Howes, 1992;Marshall, 1967), 2) are quite complex with up to 6 sonic muscles (3 pairs) in some species and deep modifications of the swimbladder, rostral vertebral bodies and associated epineurals (Parmentier et al, 2010(Parmentier et al, , 2008a(Parmentier et al, , 2006aRose, 1961), 3) are able to produce different sounds (Mann et al, 1997;Parmentier et al, 2016aParmentier et al, , 2016bParmentier et al, , 2018bParmentier et al, , 2008bSprague and Luczkovich, 2001) and have sexually dimorphic sonic systems (Ali et al, 2016;Casadevall et al, 1996;Kéver et al, 2014aKéver et al, , 2014cNguyen et al, 2008;Rose, 1961). These features clearly support the importance of sonic communication in the Ophidiiformes (Fine et al, 2018(Fine et al, , 2007Nguyen et al, 2008).…”

New insights into sound production in <I>Carapus mourlani</I> (Carapidae)

“…These results are quite surprising because both C. acus and C. mourlani possess the same soundproducing mechanism as the other Carapus and Encheliophis spp. (Courtenay and McKittrick 1970, Parmentier et al 2008, 2016.…”